An Emergent Neural Coactivity Code for Dynamic Memory

Neural correlates of external variables provide potential internal codes that guide an animal’s behaviour. Notably, first-order features of neural activity, such as single-neuron firing rates, have been implicated in encoding information. However, the extent to which higher-order features, such as multi-neuron coactivity, play primary roles in encoding information or secondary roles in supporting single-neuron codes remains unclear. Here we show that millisecond-timescale coactivity amongst hippocampal CA1 neurons discriminates distinct millisecond-lived behavioural contingencies. This contingency discrimination was unrelated to the tuning of individual neurons but instead an emergent property of their coactivity. Contingency discriminating patterns were reactivated offline after learning and their reinstatement predicted trial-by-trial memory performance. Moreover, optogenetic suppression of inputs from the upstream CA3 region selectively during learning impaired coactivity-based contingency information in CA1 and subsequent dynamic memory retrieval. These findings identify coactivity as a primary feature of neural firing that discriminates distinct behaviourally-relevant variables and supports memory retrieval.